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Abundance, Contribution, and Possible Driver of Ammonia-Oxidizing Archaea (AOA) in Various Types of Aquatic Ecosystems

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Abundance, Contribution, and Possible Driver of Ammonia-Oxidizing Archaea (AOA) in Various Types of Aquatic Ecosystems Journal of Soils and Sediments (2019) 19:2114–2125 https://doi.org/10.1007/s11368-018-2188-8 SEDIMENTS, SEC 4 • SEDIMENT-ECOLOGY INTERACTIONS • RESEARCH ARTICLE Abundance, contribution, and possible driver of ammonia-oxidizing archaea (AOA) in various types of aquatic ecosystems Weidong Wang1 & Weiyue Liu1,2 & Shanyun Wang1 & Mengzi Wang1 & Xi-En Long3 & Guibing Zhu1,2 Received: 16 July 2018 /Accepted: 4 November 2018 /Published online: 15 November 2018 # Springer-Verlag GmbH Germany, part of Springer Nature 2018 Abstract Purpose In some habitats, ammonia oxidation highly depends on the activity of ammonia-oxidizing archaea (AOA), which are therefore important for studying biogeochemical nitrogen cycling. However, the behavior and distribution of AOA in aquatic ecosystems are not well characterized, especially on a global scale. Materials and methods We sampled 66 sites across all five continents to analyze the global abundance of AOA. Ammonium oxidation rates were measured using the dicyandiamide (DCD) and octyne inhibition method to separately evaluate the contri- butions of AOA to ammonium oxidation. High-throughput pyrosequencing and phylogenetic analysis were applied to study AOA community compositions, combined with DNA-stable isotope probing (DNA-SIP). Results and discussion The archaeal amoA gene was widespread and abundant across all aquatic ecosystem types. The average abundance was 3.59 × 108 copies g−1, with the highest values in lake samples and the lowest in river samples. The AOA − −1 −1 abundance was influenced by pH. Archaeal ammonia oxidation rates were 0.81 ± 0.45 mg (NO3 -N) kg day ,corresponding to 63.75% of the total ammonia oxidation rate. Pyrosequencing analysis showed that the AOA community was dominated by the Group I.1b lineage (65.8%). Candidatus Nitrosocosmicus franklandus showed the highest positive correlation with archaeal ammonium oxidation rates and had the highest carbon use efficiency. Conclusions Abundance, activity, and community composition of AOA were highly heterogeneous. pH negatively impacted the abundance of the archaeal amoA functional gene. AOA were the main ammonia oxidators in aquatic ecosystems. Ca. N. franklandus was found to dominate archaeal ammonium oxidation. Keywords Archaeal ammonium oxidation . Activity . Biogeochemical factors . Nitrosocosmicus . Aquatic ecosystems 1 Introduction environmental problems such as eutrophication. Furthermore, sediments are the main nitrogen sink and repre- Due to the rapid growth of the world’s population, the nitro- sent biocatalytic filters for the water column above (Zhu et al. gen pollution of aquatic ecosystems (which act as nitrogen 2013; Wang et al. 2018a). Nitrification is the center of the Bsinks^) has increased dramatically, resulting in a series of biogeochemical nitrogen cycle and determines both the rate and flux of nitrogen removal (Schleper and Nicol 2010; Zhou et al. 2015;Wangetal.2018b). Ammonia oxidation, as the Responsible editor: Terrence H. Bell rate-limiting step of nitrification, has long been assumed to be Electronic supplementary material The online version of this article only conducted by ammonia-oxidizing bacteria (AOB); how- (https://doi.org/10.1007/s11368-018-2188-8) contains supplementary material, which is available to authorized users. ever, the discovery of ammonia-oxidizing archaea (AOA) challenged this assumption (Prosser 1989; Könneke et al. * Guibing Zhu 2005; Stahl and de la Torre 2012). AOA are widely distributed [email protected] throughout aquatic ecosystems, such as marine waters (Francis et al. 2005), inland saline-alkaline wetlands (Gao 1 Research Center for Eco-Environmental Sciences, Chinese Academy et al. 2018), hotsprings (Zhang et al. 2008), constructed wet- of Sciences, Beijing 100085, China lands (Su et al. 2018), and natural freshwater lakes (Liu et al. 2 University of Chinese Academy of Sciences, Beijing 100049, China 2017). As compared to AOB, which dominates nitrification in 3 Key Lab of Urban Environment and Health, Institute of Urban high ammonium nitrogen environments, AOA is known for Environment, Chinese Academy of Sciences, Xiamen 361021, China J Soils Sediments (2019) 19:2114–2125 2115 its higher specific affinity for ammonia and preference to in- environments (Weidler et al. 2008). BCandidatus habit low ammonium nitrogen environments (Martens- Nitrosocosmicus franklandus^ has first been isolated from Habbena et al. 2009; Erguder et al. 2009;Kitsetal.2017) arable soil (pH 7.5) in 2016 and belongs to the and low pH conditions (Nicol et al. 2008). Many previous BNitrososphaera sister cluster^ (Lehtovirta-Morley et al. studies suggested that AOA could outnumber AOB by at least 2016); it is capable of ureolytic growth and has a higher tol- an order of magnitude in nutrient limiting (oligotrophic) erance to nitrite and ammonia than other AOA, but a similar aquatic ecosystems, e.g., the Missouri freshwater wetlands, tolerance level compared to typical soil AOB. However, few USA (Sims et al. 2012); Chaohu Lake, China (Wang et al. studies have investigated the importance of Ca. N. franklandus 2018a), and mangrove sediments (Cao et al. 2011). The above in archaeal nitrification (Sauder et al. 2017). Hence, the contri- research results were obtained in a specific environment, and bution of Ca. N. franklandus to ammonia oxidation in aquatic few studies have focused on a wider range. However, the ecosystems should be thoroughly re-assessed. contribution of AOA to ammonia oxidation in a large range In this context, the objectives of this study are to investigate of environments has not been investigated so far (Brochier- the occurrence, distribution, and biodiversity of AOA in Armanet et al. 2008). The discovery of ubiquitous archaeal aquatic ecosystems on a global scale. To achieve this, we used ammonium oxidation greatly stimulated the view of its impor- high-throughput pyrosequencing, quantitative real-time PCR tant role in the global nitrogen cycle and considerable signif- (qPCR), and DNA-stable isotope probing (DNA-SIP) to com- icance in aquatic ecosystems (Liu et al. 2010; Wang et al. pare the abundance, contribution, and possible driver of AOA 2011). communities in various aquatic ecosystems. Ammonia oxidation is catalyzed by ammonia monooxygenase, which is composed of the three subunits amoA, amoB, and amoC. Among them, amoA, encoding 2 Materials and methods the α-subunit of ammonia monooxygenase, is widely used as marker for bacterial and archaeal ammonia oxidizers. 2.1 Study sites Studies have classified AOA as a novel archaeal phylum of the Thaumarchaeota lineage (Brochier-Armanet et al. 2008; We collected and investigated a total of 66 sediment samples Spang et al. 2010), which separates them from the phyla from aquatic ecosystems, including lakes, rivers, paddy fields, Euryarchaeote and Crenarchaeota. Ammonia-oxidizing ar- reservoirs, and swamps, from eight countries of all five conti- chaea form five distinct phylogenetic clades, namely the nents. Details of the sampling sites, including location, eleva- BNitrosopumilus cluster^ (also called group I.1a), the tion, sediment type, and temperature are shown in Fig. 1 and BNitrososphaera cluster^ (also called group I.1b), the Table S1 (Electronic Supplementary Material (ESM)). Surface BNitrososphaera sister cluster,^ the ‘Nitrosotalea cluster,^ sediment samples (0–10 cm) were collected from each sam- and the BNitrosocaldus cluster (ThAOA)^ (Pester et al. pling site in triplicate, sealed in sterile plastic bags, and imme- 2012). Generally, AOA from the sediments and water of the diately transported on ice to the laboratory. A portion (10 g) of ocean are clustered in group I.1a, while terrestrial AOA are each of the fresh samples was stored at − 80 °C for DNA distributed in the group I.1b branch (Nicol and Schleper extraction and other molecular analyses. A further portion 2006). The cluster ThAOA is distinct from the other branches (100 g) was air-dried and sieved through a 2-mm mesh for and mostly occurs in hot springs and high-temperature physicochemical analyses. The remaining samples were Fig. 1 Location of the sampling sites. Circles of different colors represent different aquatic ecosystem types, and the number in the circle represents the number of samples. In total, 66 sediment samples were collected from eight countries in five continents 2116 J Soils Sediments (2019) 19:2114–2125 incubated at in situ temperature (9–29 °C) to determine mi- generated by a 10-fold dilution of a plasmid with the amoA crobial activities. gene of a known concentration. The detection limit of the qPCR was 1.00 × 103 copies g−1. The results with an amplifi- 2.2 Analysis of environmental variables cation efficiency and a correlation coefficient (R2) above 95% and 0.98, respectively were employed. All tests were per- + − Ammonium (NH4 ) and nitrite plus nitrate (NOx )wereex- formed in triplicate. tracted from the fresh sediments with 2 M KCl solution and measured using a continuous flow analyzer (SAN plus, Skalar 2.5 Measurement of ammonia-oxidizing activity Analytical B.V. the Netherlands). Total nitrogen (TN), total carbon (TC), total sulfur (TS), and total phosphorus (TP) con- Out of a total of 66 samples, 15 representative samples were tents were measured using an elemental analyzer selected for the determination of the ammonia oxidation rate. (ELEMENTAR, Germany). The pH was determined after These 15 samples covered five continents and three types of mixing with water at a ratio (sediment/water) of 1:5, and total aquatic ecosystems. Laboratory
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